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MINI REVIEW
published: 21 April 2015
doi: 10.3389/fpls.2015.00280
Edited by:
David W. M. Leung,
University of Canterbury, New Zealand
Reviewed by:
Ruediger Hell,
University of Heidelberg, Germany
Gijs A. Kleter,
Wageningen University and Research
Centre, Netherlands
*Correspondence:
Mario Malagoli,
Department of Agronomy, Food,
Natural Resources, Animals and the
Environment, University of Padova,
Agripolis, 35020 Legnaro Padova,
Italy
mario.malagoli@unipd.it
Specialty section:
This article was submitted to
Plant Biotechnology,
a section of the journal
Frontiers in Plant Science
Received: 31 October 2014
Paper pending published:
11 December 2014
Accepted: 08 April 2015
Published: 21 April 2015
Citation:
Malagoli M, Schiavon M, dall’Acqua S
and Pilon-Smits EAH (2015) Effects of
selenium biofortification on crop
nutritional quality.
Front. Plant Sci. 6:280.
doi: 10.3389/fpls.2015.00280
Effects of selenium biofortification
on crop nutritional quality
Mario Malagoli 1*, Michela Schiavon 1, Stefano dall’Acqua 2and Elizabeth A. H.
Pilon-Smits 3
1Department of Agronomy, Food, Natural Resources, Animals and the Environment, University of Padova, Padova,
Italy, 2Department of Pharmaceutical and Pharmacological Sciences, University of Padova, Padova, Italy, 3Department of
Biology, Colorado State University, Fort Collins, CO, USA
Selenium (Se) at very low doses has crucial functions in humans and animals. Since plants
represent the main dietary source of this element, Se-containing crops may be used
as a means to deliver Se to consumers (biofortification). Several strategies have been
exploited to increase plant Se content. Selenium assimilation in plants affects both sulfur
(S) and nitrogen (N) metabolic pathways, which is why recent research has also focused
on the effect of Se fertilization on the production of S- and N- secondary metabolites with
putative health benefits. In this review we discuss the function of Se in plant and human
nutrition and the progress in the genetic engineering of Se metabolism to increase the
levels and bioavailability of this element in food crops. Particular attention is paid to Se
biofortification and the synthesis of compounds with beneficial effects on health.
Keywords: selenium, plant biofortification, food, nutritional quality, secondary metabolites
The Importance of Selenium to Human and Animal Health
Selenium is an essential trace element for humans and animals, and some organic forms like methyl-
selenocysteine (MeSeCys) appear to be particularly effective sources of dietary Se. Selenium is
incorporated as selenocysteine (SeCys) at the active site of a wide range of selenoproteins involved in
major metabolic pathways, such as thyroid hormone metabolism, antioxidant defense and immune
function (Rayman, 2012). Low intake of Se in the diet may cause a number of diseases, including
heart diseases, hypothyroidism, reduced male fertility, weakened immune system and enhanced
susceptibility to infections and cancer (Hatfield et al., 2014; Roman et al., 2014). Selenium deficiency
is thought to affect 800 million people worldwide. In livestock, Se deficiency is also responsible for
the white muscle disease, with clinical signs that include lesions in skeletal and/or heart muscle.
Selenium supplementation of grazing livestock is mandatory in USA and Canada, because there is a
marked seasonal and soil-dependent variation in their Se nutrition. For most of the world human and
livestock population, vegetables are an important source of Se intake. Thus, increasing Se content in
food crops offers an effective approach to reduce the Se deficiency problem in humans and animals.
Selenium Transport and Assimilation in Plants
While there is no proof of essentiality for Se in plants (Pilon-Smits et al., 2009), Se is readily taken up
by plants in the form of selenate through the sulfate transporters (Figure 1). Due to their chemical
similarities (Shibagaki et al., 2002; El Kassis et al., 2007), Se and sulfur (S) compete for the same
transporters, and Se uptake is generally limited by high S levels. After uptake, selenate can access
the sulfate assimilation pathway and be reduced via selenite to selenide (Figure 1). Selenide can be
incorporated into the S-analog amino acid selenocysteine (SeCys), which may further be converted
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Malagoli et al. Se biofortification for food quality
FIGURE 1 | Selenate (and sulfate) uptake and assimilation in plants.
Selenate is taken up by sulfate transporters (Sultr), and activated by ATP
sulfurylase for further assimilation to selenocysteine (SeCys). SeCys can be
further metabolized to selenomethionine and to volatile dimethylselenide.
Non-hyperaccumulators often store selenate, because APS is a rate-limiting
enzyme. Its overexpression resulted in enhanced Se accumulation and
tolerance. Selenium hyperaccumulators methylate SeCys via the enzyme SeCys
methyltransferase (SMT) and accumulate methyl-SeCys, a non-protein
aminoacid. Methyl-SeCys may also be converted to volatile dimethyldiselenide.
Expression of SMT in non-hyperaccumulators resulted in enhanced Se
accumulation (as methylSeCys) and tolerance. Sulfur and nitrogen metabolic
pathways interact at the level of -acetylserine. Changes in S assimilation
induced by Se can in turn affect N metabolism, with respect to protein and
amino acid synthesis. Amino acids methionine, phenylalanine (Phe), tyrosine
(Tyr), and tryptophan (Trp) are precursors of glucosinolates (GLS) and Phe is a
precursor for phenolics. Variation in the synthesis of these amino acids influence
the production of nutraceutical compounds [glucosinolates (GLS) and
phenolics]. In addition, Se can directly induce production of phenolics in plants.
in three enzymatic steps to selenomethionine (SeMet; for a review,
see Sors et al., 2005). The mistaken insertion of these Se-amino
acids into proteins instead of cysteine and methionine may cause
metabolic dysfunction (Sabbagh and Van Hoewyk, 2012). Incor-
poration of Se into proteins may be avoided by diverting Se
to other, less toxic forms. Some plants accumulate the non-
protein organic Se-compounds methylselenocysteine (MeSeCys),
γ-glutamyl-MeSeCys and/or selenocystationine, sometimes to
very high tissue levels without ill effects (Terry et al., 2000).
Selenium can also be volatilized from plants in the forms of
dimethylselenide or dimethyldiselenide, which are produced from
SeMet and methyl-SeCys, respectively (Figure 1). The different
selenocompounds found in plants have different toxicity levels
and different nutritional value, with organic forms generally being
more efficient in Se biofortification. Therefore, it is important to
know which forms of Se are present in plant material used for
nutritional supplementation. If we know which enzymes control
the various metabolic steps it is also possible to genetically engi-
neer more nutritious forms of Se in crop plants by enhancing the
levels of critical enzymes.
Selenium Biofortification Efforts
Selenium is chemically analogous to S and therefore accumulated
by all plants to some extent, in all plant parts. The plant Se levels
found in nature and in crops depends on soil Se abundance and
the levels of competing S compounds (Figure 2). In addition,
plant Se concentrations at a given seleniferous site, i.e., a site
containing more than 1 (and up to 100) mg Se kg−1soil, may
vary over 100-fold between plant species (Galeas et al., 2007).
Different plant species differ with respect to their capacity to accu-
mulate Se, which likely correlates with their expression levels of
sulfate transporters. Plant species also vary with respect to which
forms of Se they accumulate due to the presence and activity of
various S/Se metabolic enzymes. Selenium biofortification efforts
may make use of this natural variation between plant species,
and choose crop species that naturally tend to contain higher Se
(and S) levels, such as Brassica and Allium species (Terry et al.,
2000). Since Se biofortification is most effective when organic Se
is supplied, plant species known to accumulate organic forms of
Se may be preferred, including broccoli and garlic (Lyi et al., 2005;
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Malagoli et al. Se biofortification for food quality
FIGURE 2 | Processes related to Se in the soil-plant system, relevant for Se biofortification. Selenate is taken up from soil and assimilated (particularly by Se
hyperaccumulators) to organic forms of Se. Some Se is accumulated and some volatiled as nontoxic dimethyl(di)selenide.
Hsu et al., 2011). Care has to be taken to not supply unnecessary
S in Se-fortified crop production, since S will reduce Se uptake. In
soils where Se levels are very low, as e.g., in Finland, the United
Kingdom, parts of China, and New Zealand (Chen et al., 2002;
Broadley et al., 2006; Alfthan et al., 2014), it is not enough to
just plant Se-accumulating crop species, but also necessary to
provide inorganic Se as fertilizer for the crop. This practice is
in effect in Finland since the 1980s, and has led to significantly
enhanced blood Se levels in the general population (Alfthan et al.,
2014). Whether this is concomitant with positive health effects
remains to be investigated; a complicating factor is that there is
no reference population. In Se-deficient areas of China, too, Se
biofortification of crops is practiced to prevent the devastating
Keshan disease still prevalent in vast areas, which is characterized
by cardiomyopathy caused by Se deficiency (Bañuelos et al., 2013).
Genetic Engineering of Plant Se
Metabolism and its Potential
for Biofortification
Genetic engineering, which has been shown to enhance Se accu-
mulation, tolerance, and volatilization by plants, has focused
on S-related enzymes. First, overexpression in Brassica juncea
of ATP sulfurylase (APS), a key enzyme for selenate-to-selenite
transition, resulted in enhanced selenate reduction: the transgenic
APS plants accumulated organic Se (likely methyl-SeCys) when
supplied with selenate, while wildtype controls accumulated sele-
nate (Pilon-Smits et al., 1999). The APS transgenics accumulated
and tolerated more Se as well (Figure 1). In another approach,
SeCys methyltransferase (SMT) was overexpressed in A. thaliana
and B. juncea (Ellis et al., 2004; LeDuc et al., 2004). The SMT
transgenics showed enhanced Se accumulation, and the form
was methyl-SeCys (Figure 1). In both APS and SMT transgenics
more Se is accumulated, and their form of Se is more suitable for
biofortification (Figure 2).
When APS and SMT B. juncea transgenics were crossed to
create double-transgenic plants, these accumulated up to 9 times
higher Se levels than wild type (LeDuc et al., 2006). Most of the
Se in the double transgenics was in the form of methyl-SeCys:
the APSxSMT plants accumulated up to eightfold more methyl-
SeCys than wild type and nearly twice as much as the SMT
transgenics.
When grown on naturally seleniferous soil in a greenhouse
pot experiment, the APS transgenics accumulated Se to threefold
higher levels than wildtype B. juncea (Van Huysen et al., 2004).
In two field experiments carried out on selenate-contaminated
soil in central California, the APS transgenics accumulated four-
fold higher Se levels than wildtype B. juncea, and SMT trans-
genics showed twofold higher Se levels (Bañuelos et al., 2005,
2007). Biomass production was comparable for the different plant
types. Thus, genetic engineering has produced new genotypes of
B. juncea with enhanced Se accumulation and higher levels of
nutritious organic Se, all promising for use as Se-fortified foods.
In addition to the S assimilation enzymes, sulfate trans-
porters may be potential targets of genetic engineering; selenate
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Malagoli et al. Se biofortification for food quality
transporters from Se hyperaccumulators will be particularly inter-
esting in this respect.
Effects of Se Biofortification on Secondary
Plant Compounds
Variations in plant S uptake and assimilation induced by Se may
cause changes in the synthesis of S-secondary compounds with
nutritional value, such as glucosinolates (GLS), which function
in plant defense against insects and herbivores (Figure 1). The
hydrolysis of GLS within cells produces isothiocyanates, which
act as cancer-preventing agents in mammals (Dinkova-Kostova,
2013).
Because S nutrition is strictly associated with N metabolism,
Se can exert an additional effect on the synthesis of proteins and
amino acids, as well as on N-secondary compounds with free
radical scavenging activities, like phenolics (Figure 1). Amino
acids such as methionine, phenylalanine (Phe), tyrosine (Tyr) and
tryptophan (Trp) are precursors of GLS. Furthermore, Phe is the
substrate for phenolics biosynthesis. Variation in the synthesis
of these amino acids influence the production of both types of
beneficial compounds.
Several studies examined how Se enrichment of plants affects
their content in these phytochemicals (Robbins et al., 2005; Bar-
ickman et al., 2013; Schiavon et al., 2013). Tomato (Solanum
lycopersicon L.) plants and Brassica species in particular, contain
high levels of phenolic compounds. Additionally, Brassica spp. are
rich in glucosinolates (GLSs).
In broccoli (Brassica oleracea L.), Se fertilization was shown
to reduce the amount of total phenolic acids, without altering
the profile distribution of specific compounds (Robbins et al.,
2005). In contrast, Se at low dosages (5 and 10 µM) increased
the leaf phenolic content of hydroponically grown tomato plants
(Schiavon et al., 2013). Furthermore, the supply of selenate via
foliar spray at 2 and 20 mg Se plant−1resulted in Se-biofortified
tomato fruits, with enhanced levels of the antioxidant flavonoids
naringenin, chalcone and kaempferol (Schiavon et al., 2013).
Selenium fertilization may also affect the levels of GLS, a class
of secondary plant S compounds. GLS may have anticarcinogenic
properties, based on studies using experimental in vitro and in vivo
models, but can also cause toxicity at elevated levels (Assayed and
Abd El-Aty, 2009). The presence of GLS and GLS-metabolites at
high level in animal feed can cause the decrease in growth and pro-
duction, affecting organs such as liver, kidney, lungs and inducing
morphological and physiological changes of thyroid (Tripathi and
Mishra, 2007). Robbins et al. (2005) reported a weak reduction
of indole, aliphatic, total glucosinolates, and glucoraphanin after
Se fertilization, and a strong fall of sulforaphane production. A Se-
related decrease of these compounds in broccoli was also observed
by Barickman et al. (2013), but high levels of GLSs could be
maintained with Se concentration lower than 0.8 mg L-1 or by
increasing S concentration in the medium. Exposing plants to
low Se concentrations can promote S uptake and assimilation
in some species, including B. juncea (Harris et al., 2014), thus
potentially increasing the level of S-organic compounds. However,
while upregulating S uptake and assimilation, Se treatment was
also found to upregulate genes involved in GLSs breakdown in
A. thaliana (Van Hoewyk et al., 2008).
Recently, Ávila et al. (2013, 2014) showed the reduction of
GLSs in the florets of broccoli treated with selenate, whereas
in the sprouts GLS levels were not affected. Moreover, sprouts
contained nearly sixfold higher content of the potent anticancer
glucoraphanin than florets. Se-enriched sprouts were expected
to exhibit greater potential anticancer activity because of high
accumulation of SeMCys with similar glucosinolate production.
Brassica crops supplied with selenate were able to form selenoglu-
cosinolates, with a methylselenoalkyl group that was likely derived
from selenomethionine (Matich et al., 2012). Selenoglucosinolates
accounted for 60% of the concentrations of their S analogs (Matich
et al., 2012). The production of selenoglucosinolates following Se-
fertilization has implications for human health, as the synthetic
Se-containing isothiocyanates are reported to be more potent
anticancer compounds than their S counterparts (Emmert et al.,
2010). As mentioned, the Se-GLS and/or GLS content must be
monitored when plants or their residues are used for human or
animal consumption, to avoid potential toxicity effects.
Future Prospects
Studies so far indicate that it is possible to maximize multiple
bioactive components in a single plant. However, because in some
cases the accumulation of Se may interfere with the production
of some classes of phytochemicals, the Se biofortification pro-
grams must consider the interactions between Se and the main
metabolic pathways of the plant. Particular attention should be
paid to the reciprocal effects of Se and S on their accumulation and
assimilation into organic compounds. In this context, managing S
concentration during Se fertilization to vary S:Se ratios could be
envisioned as a strategy to increase Se to beneficial dietary levels
in plants without compromising GLS and other health-promoting
compound contents.
An interesting new area of research involves the use of plant-
microbe interactions to enhance Se biofortification. Another
avenue to explore is the cultivation of Se fortified crops on
seleniferous soil, thereby improving the amenity of that soil for
further agriculture, and using the produced biomass to fortify the
diets of people (and their livestock) in Se-deficient areas. Finally,
since different plant species appear to be able to influence their
neighboring plants’ Se accumulation and perhaps speciation (El
Mehdawi et al., 2012), it will be interesting to further explore the
potential of various co-cropping techniques to optimize crop Se
biofortification and nutritional quality.
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Conflict of Interest Statement: The authors declare that the research was con-
ducted in the absence of any commercial or financial relationships that could be
construed as a potential conflict of interest.
Copyright © 2015 Malagoli, Schiavon, dall’Acqua and Pilon-Smits. This is an open-
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Frontiers in Plant Science | www.frontiersin.org April 2015 | Volume 6 | Article 2805
